How Mycorrhizal Associations Influence Orchid Distribution and Population Dynamics Taiqiang Li, Shimao Wu, Wenke Yang, Marc-André Selosse, Jiangyun Gao

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Taiqiang Li, Shimao Wu, Wenke Yang, Marc-André Selosse, Jiangyun Gao. How Mycorrhizal Associ- ations Influence Orchid Distribution and Population Dynamics. Frontiers in Plant Science, Frontiers, 2021, 12, pp.647114. ￿10.3389/fpls.2021.647114￿. ￿hal-03235972￿

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How Mycorrhizal Associations Influence Orchid Distribution and Population Dynamics

Taiqiang Li 1,2, Shimao Wu 1,2, Wenke Yang 1,2, Marc-André Selosse 1,2,3,4 and Jiangyun Gao 1,2*

1 Yunnan Key Laboratory of Plant Reproductive Adaptation and Evolutionary Ecology, Yunnan University, Kunming, China, 2 Laboratory of Ecology and Evolutionary Biology, Yunnan University, Kunming, China, 3 Institut de Systématique, Évolution, Biodiversité, UMR 7205, CNRS, MNHN, UPMC, EPHE, Muséum National d’Histoire Naturelle, Sorbonne Universités, Paris, France, 4 Department of Plant Taxonomy and Nature Conservation, Faculty of Biology, University of Gdańsk, Gdańsk, Poland

Orchid distribution and population dynamics are influenced by a variety of ecological factors and the formation of holobionts, which play key roles in colonization and ecological community construction. Seed germination, seedling establishment, reproduction, and survival of orchid species are strongly dependent on orchid mycorrhizal fungi (OMF), with mycorrhizal cheating increasingly observed in photosynthetic orchids. Therefore, changes in the composition and abundance of OMF can have profound effects on orchid distribution and fitness. Network analysis is an important tool for the study of interactions between Edited by: Nadia Lombardi, plants, microbes, and the environment, because of the insights that it can provide into Università degli Studi di Napoli the interactions and coexistence patterns among species. Here, we provide a Federico II, Italy comprehensive overview, systematically describing the current research status of the Reviewed by: Lawrence W. Zettler, effects of OMF on orchid distribution and dynamics, phylogenetic signals in orchid–OMF Illinois College, United States interactions, and OMF networks. We argue that orchid–OMF associations exhibit Franck Richard, complementary and specific effects that are highly adapted to their environment. Such UMR5175 Centre d’Ecologie Fonctionnelle et Evolutive (CEFE), specificity of associations may affect the niche breadth of orchid species and act as a France stabilizing force in plant–microbe coevolution. We postulate that network analysis is *Correspondence: required to elucidate the functions of fungal partners beyond their effects on germination Jiangyun Gao [email protected] and growth. Such studies may lend insight into the microbial ecology of orchids and provide a scientific basis for the protection of orchids under natural conditions in an efficient Specialty section: and cost-effective manner. This article was submitted to Plant Symbiotic Interactions, Keywords: orchid mycorrhizal fungi, orchid performance, complementary selection, environmental variables, a section of the journal evolutionary constraints, mycorrhizal networks, keystone taxa Frontiers in Plant Science

Received: 29 December 2020 Accepted: 13 April 2021 Published: 07 May 2021 INTRODUCTION Citation: Mycorrhizal associations play a key role in generating and maintaining plant diversity. Such Li T, Wu S, Yang W, Selosse M-A and associations not only enhance the acquisition, transmission, and cycling of nutrients in Gao J (2021) How Mycorrhizal Associations Influence Orchid plants, but also mediate interactions among different plants and between plants and Distribution and Population Dynamics. non-mycorrhizal fungi (Tedersoo et al., 2020). A growing body of research suggests that Front. Plant Sci. 12:647114. mycorrhizal symbionts are important drivers of biogeographic patterns, distributions, community doi: 10.3389/fpls.2021.647114 dynamics, and the health of plants, mediated by their effects on dispersal and coexistence

Frontiers in Plant Science | www.frontiersin.org 1 May 2021 | Volume 12 | Article 647114 Li et al. Roles of OMF in Orchid Distribution of species (Delavaux et al., 2019; Trivedi et al., 2020). For These clues strongly suggest that environmental factors may example, ectomycorrhizae (EcM) interact with pathogenic indirectly affect orchid distribution and population dynamics fungi to maintain community diversity (Chen et al., 2019a). by driving niche partitioning in OMF communities. Similarly, The family Orchidaceae is extremely diverse (with 28,000+ OMF can decompose carbon and nitrogen sources in soil species), widely distributed across highly heterogeneous organic matter and transfer them to the associated host orchids microenvironments, and exhibits large spatiotemporal variation (Rasmussen, 1995). In addition, orchids often share EcM with in population size (Givnish et al., 2016; Fay, 2018; Djordjević neighboring trees, hence orchid mycorrhiza may mediate the and Tsiftsis, 2020). A common feature of all orchids is their significant effect of vegetation types on orchid niche partitioning obligatory dependence on orchid mycorrhizal fungi (OMF), (Waterman and Bidartondo, 2008; Jacquemyn et al., 2016a). which makes the presence of suitable OMF or co-dispersal Orchid fungi are divided into OMF and orchid with partners a prerequisite for the establishment and non-mycorrhizal fungi (ONF) based on whether or not functional maintenance of orchid populations (Dearnaley et al., 2012; pelotons are present in cortical cells. OMF include at least 17 McCormick and Jacquemyn, 2014). Mycorrhizal symbiosis is families of basidiomycetes and five families or genera of especially important for plants associated with OMF and EcM, ascomycetes (Dearnaley, 2007; Dearnaley et al., 2012). as they often have high mycorrhizal specificityPõlme ( et al., Tulasnellaceae, Ceratobasidiaceae, and Serendipitaceae are most 2018). Most species of EcM fungi exhibit short-distance commonly known as rhizoctonia-type Basidiomycetes. dispersal and therefore, have limited ranges of distribution Basidiomycetes and Ascomycetes are relatively abundant in the (Sato et al., 2012; Tedersoo et al., 2020). Although the major tree roots of forest ecosystems and cultivated species worldwide mycorrhizal partners of terrestrial orchids appear to favor a (Cregger et al., 2018; Wang et al., 2019a; Trivedi et al., 2020), cross-scale distribution with specificity ranging from wide to and are commonly associated with orchids as well. Interestingly, very narrow (Jacquemyn et al., 2017; Swarts and Dixon, 2017), a large proportion of ascomycetes associated with orchids are comparatively little is known about the diversity and ONF. For example, Helotiales endophytes are the dominant biogeography of the associated mycorrhizae of epiphytic orchids. group of ONF associated with host orchids in different habitats Therefore, the interaction between OMF and orchids is a as well as major players in plant–fungus associations in a key factor determining orchid distribution and development, variety of forest ecotypes (Toju et al., 2013; Jacquemyn et al., and diversity of OMF has a strong impact on the niche and 2016a, 2017). Previous studies have identified more than 110 life cycle of host orchids. For instance, low OMF diversity genera of ONF, including 76 genera of ascomycetes and 32 and high heterogeneity in OMF community composition may genera of basidiomycetes (Ma et al., 2015). Although ONF lead to weak growth of orchid populations (Kaur et al., 2020). are often overlooked, recent studies have highlighted their Orchids exhibit astonishing morphological characteristics, importance in the promotion of orchid seed germination and such as labella and modified petals, that indicate their substantial performance as well as changes in the composition of key adaptability to the environment (Zhang et al., 2018). On one chemicals such as sugars. Moreover, they also play a role in hand, interactions with specific pollinators promote the mobilizing soil nutrients in the rhizosphere to improve orchid reproduction of orchids; on the other hand, symbiotic fungi viability and environmental adaptability, and serve as new are required for soil exploitation (Selosse, 2014). Greater sources of phytochemicals and bioactive substances to protect environmental heterogeneity and a wider range of resource the host from soil pathogens. Hence, these ONF provide the availability usually contribute to the increase of orchid species plants with promising medicinal and agricultural breeding diversity (Schödelbauerová et al., 2009; Traxmandlová et al., prospects (Chen et al., 2006; Yuan et al., 2009; Aly et al., 2018). Thus, untangling the role of environmental conditions 2010; Novotná et al., 2018; Sisti et al., 2019; Hajong and Kapoor, in determining the distribution and abundance of orchids is 2020; Wu et al., 2020). Furthermore, ONF may interact with a prerequisite for effective conservation of these species. Recently, OMF to influence the distribution and population dynamics Djordjević and Tsiftsis (2020) systematically sorted out the of orchids. Therefore, the diversity and functionality of ONF effects of environmental factors on the distribution, abundance, should be further explored to gain insight into the associations and richness of orchids. For instance, rainfall and light regime between orchids and fungi as a whole. In addition, studying in the habitat are closely related to the flowering patterns and how ONF and OMF make rational use of the ecological niches population dynamics of orchids (Wells and Cox, 1991; Jacquemyn in orchid rhizospheres (i.e., their coexistence mechanism) and et al., 2010a); physical and chemical properties of soil (such the correlation between their distribution and the phylogenetic as pH, soil moisture, nutrients, etc.) significantly affect the eigenvectors of orchid species could help us better understand performance of orchid populations (Stuckey, 1967; Tsiftsis et al., orchid mycorrhizal ecology. We believe that the development 2012). Interestingly, there is growing evidence supports that of molecular methods and genomics techniques enables the coexisting orchid species usually exhibit strongly spatially simultaneous consideration of both OMF and ONF in mycorrhizal segregated distribution patterns due to strong clustering within ecology. This may breed a more complete and informative individual species and small overlap between species, and that fungal network that can more accurately predict their association they are often associated with different OMF communities, with environmental variables, which may be a key to igniting which are largely explained by differences in soil moisture a new wave of research into orchid mycorrhizae. and pH (e.g., Jacquemyn et al., 2007, 2012, 2014, 2015a; The thousands of complex and highly dynamic interactions Waud et al., 2017; Chen et al., 2019b; Kaur et al., 2019). between plants, microbiomes, and the environment can

Frontiers in Plant Science | www.frontiersin.org 2 May 2021 | Volume 12 | Article 647114 Li et al. Roles of OMF in Orchid Distribution be analyzed using ecological networks that play pivotal roles of ecosystem function. Network hubs are further defined as in associations between OMF, EcM, and arbuscular mycorrhizae keystone taxa due to their high connectivity within these (AM) fungi, and are often used as black boxes to study the networks, and have more important functional attributes and transfer of carbon signals across hosts (Banerjee et al., 2018; high interpretation rates on the dynamics of plant microorganisms Tedersoo et al., 2020). Modular analysis within these networks (Deng et al., 2012; Cavieres et al., 2014; Banerjee et al., 2018; can be used to identify key microbial groups that are closely Ma et al., 2020). Thus, they can be used to manipulate the related to plant growth and yield. Additionally, the topological function of the microbiome or predict changes in its community roles of the species included in complex networks can composition. A query of the Web of Science core database be simplified into four categories based on within-module using the keyword “orchid mycorrhizal network” retrieved a connectivity (Zi) and among-module connectivity (Pi; total of nine articles (as of 15 October 2020), focusing mainly Figure 1A). Connectors, module hubs, and network hubs are on the interaction between epiphytic orchids in tropical systems considered ecosystem engineers, which have significant impact or terrestrial orchids in temperate systems and OMF. The on the assembly of communities and can support higher levels methods, ecological premise and revealed network architecture

AB

C

D

FIGURE 1 | (A) z–P plot depicting the role of each species in the interaction network. Peripherals might represent specialists whereas module hubs and connectors are close to generalists and network hubs are supergeneralists. (B,C) Local citation score (LCS) and global citation score (GCS) citation diagrams of all orchid mycorrhizal network research papers retrieved from the core Database of Web of Science. Each circle represents a research article. The numbers in the circle are the LCS (B) and GCS (C) of the corresponding literature, and the size of the circle is proportional to citation scores. Arrows indicate cross-references between the studies. (D) Definition and classification of microbial taxa: (i) Always abundant taxa (AAT), operational taxonomic units (OTUs) with abundance always≥ 1% in all samples; (ii) Always rare taxa (ART), OTUs with abundance always <0.01% in all samples; (iii) Moderate taxa (MT), OTUs with abundance between 0.01 and 1% in all samples; (iv) Conditionally rare taxa (CRT), OTUs with abundance <0.01% in some samples and below 1% in all samples; (v) Conditionally abundant taxa (CAT), OTUs with abundance greater than 0.01% in all samples and ≥1% in some samples but never rare (<0.01%); and (vi) Conditionally rare and abundant taxa (CRAT), OTUs with abundance varying from rare (≤0.01%) to abundant (≥1%).

Frontiers in Plant Science | www.frontiersin.org 3 May 2021 | Volume 12 | Article 647114 Li et al. Roles of OMF in Orchid Distribution in the retrieved articles are described in Supplementary Table S1. EFFECTS OF OMF ABUNDANCE ON We used the HistCite software to analyze the citation network ORCHID DISTRIBUTION and calculate the local citation score (LCS) and global citation score (GCS) from the retrieved articles (Figures 1B,C). In To our knowledge, no reports show that the distribution of general, research on the mycorrhizal network of orchids appears orchids at large scales is restricted by OMF. While Hemrová to be insufficient, greatly restricting our understanding of the et al. (2019) suggested that fungal symbionts are the main stability and persistence of the species-rich orchid community. driving forces for the distribution of forest orchids at the Hence, in this study, we summarize the effects of OMF on landscape scale based on germination experiments and species orchid distribution and population dynamics, elucidate OMF distribution models integrating multiple habitat characteristics, networks and the phylogenetic relationships in orchid–OMF they did not find molecular evidence for OMF diversity. A interactions. More specifically, we would like to discuss the possible explanation for this is that OMF has a wide biogeographic progress in these three aspects to preliminarily clarify the distribution, and some major branches have been witnessed following two issues: (1) the mutual selection mechanism of on a broad landscape scale (Jacquemyn et al., 2017). Hence, orchid–OMF and the role of ecology and evolution in this the distribution of OMF assemblages per se may not be a pattern? and (2) the relative importance of nestedness and limiting factor for the distribution of orchids. However, extensive modularity in orchid mycorrhizal networks? Finally, in the studies sampling orchids across continents would be required “Prospects” section, we focus on the functional roles of rare to determine whether the total fungal community enlarges or groups and discuss several key issues in symbiosis that could reduces the distribution of host orchids on the landscape scale. benefit from the advancement of OMF network research. Studies on the local restriction of orchid distribution by OMF Collectively, we summarize the results or conclusions of some abundance include at least nine reports covering 13 specialized case studies related to the target topic, and attempt to focus orchids (reviewed in McCormick et al., 2018). Most results on the emerging patterns that are more consistent in these demonstrate that the germination percentage of seeds is higher summaries. However, it should be noted that the network near adult orchids where OMF abundance tends to be greater. perpective applies mainly to tropical orchids, and more datasets In addition, some studies show significant positive correlations are needed to expand other biomes. Through this review, between mycoheterotrophic orchid abundance and OMF we hope to direct attention toward the insufficiently explored abundance, strongly suggesting that OMF affects the abundance field of orchid–fungus mutualism, and encourage the use of of orchids (McCormick et al., 2009). However, current evidence beneficial fungal groups for protection of endangered orchids. showing the influence of OMF abundance on the distribution of orchids is mainly based on seed germination and protocorm EFFECTS OF OMF ON ORCHID development (McCormick et al., 2012, 2016, 2018; McCormick and Jacquemyn, 2014). Subsequent studies on the later DISTRIBUTION AND POPULATION developmental stages of orchids might unravel more information. DYNAMICS Most orchids experience carbon restrictions during nutrient dormancy. During this phase, orchids require fungi to provide The distribution and abundance of orchid populations are nutrients, and the recovery from dormancy is proposed to curtailed by biotic and abiotic factors. These include latitude, be linked to the local abundance of appropriate OMF (Rock- macroclimate, area size, and evolutionary history at the large Blake et al., 2017; McCormick et al., 2018; Shefferson et al., landscape scale, soil characteristics, light conditions, substrate 2018). Therefore, OMF abundance may affect the apparent types, degree of disturbance, pollinating insects, and seed density of orchid populations by affecting the dormancy production and dispersal at the local landscape scale, while process, thereby affecting the population characteristics and the effects of altitude, soil moisture, and pH may span both reproductive success. At the same time, OMF inoculation scales (McCormick and Jacquemyn, 2014; Djordjević et al., experiments revealed that the introduction of OMF in areas 2016; Traxmandlová et al., 2018; Tsiftsis et al., 2019; Djordjević without orchids but near existing orchid populations can and Tsiftsis, 2020). The influence of these factors may depend be successful, so that OMF abundance may also increase on the spatiotemporal scale in consideration. Although orchids seed germination and the protocorm formation rate (McCormick have dust-like seeds that generally lack nutrients, OMF play et al., 2012, 2016). Interestingly, the relationship between the a critical role in seed dispersal and germination, establishment OMF abundance and the distribution of orchids suggests that of new seedlings, and soil niche partitioning of their lifelong the location of adult orchids determines the richness and host orchid (McCormick et al., 2006, 2018; Selosse, 2014; abundance of OMF to some extent. In addition, several reports Tedersoo et al., 2020). In natural habitats, microhabitats rich demonstrate that fungi obtain nutrients from autotrophic in OMF generally facilitate more seed germination and seedling orchids (Cameron et al., 2006; Hynson et al., 2009; Liebel establishment, and more orchids tend to grow in areas with et al., 2015; Yeh et al., 2019). Therefore, we cannot rule out richer distribution of OMF. As a result, changes in OMF the possibility that the abundance of OMFs may be caused composition, abundance, and evenness may greatly influence by the density of autotrophic orchids. Furthermore, it is the fitness of orchids, which in turn affects the distribution essential to design more tests to explore factors controlling and community composition of orchids (McCormick and the abundance of OMF and their impact on individuals and Jacquemyn, 2014; Waud et al., 2016a; McCormick et al., 2018). populations of orchids.

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EFFECTS OF OMF IDENTITY AND In addition to the distribution, abundance, and identity of SPATIOTEMPORAL VARIABILITY ON OMF, spatiotemporal variation in OMF may more important ORCHID DISTRIBUTION AND factor in determining the distribution and population dynamics of orchids. The high spatiotemporal turnover rate of OMF may POPULATION DYNAMICS also reduce competition for resources, via niche separation, by promoting the coexistence of more orchid species in the natural Most orchids are combined with different OMF in different environment. This is corroborated by several studies on the habitats or climatic conditions, indicating that beneficial OMFs coexistence of terrestrial orchids that use a combination of spatial can vary across these conditions (Martos et al., 2012; Jacquemyn point pattern analysis and OMF phylogenetic analysis. These et al., 2016a,b; Duffy et al., 2019; Xing et al., 2020a). Germination studies have revealed that coexisting orchid species have different and growth promotion tests have largely shown that OMF OMF communities with little overlap over fine spatial scales, and exhibit some specificity (e.g., Zi et al., 2014; Rasmussen et al., that individual orchid species commonly occur as high-density 2015; Meng et al., 2019; Zhang et al., 2020), while some studies clusters, displaying high local dominance (Jacquemyn et al., 2012, have suggested that only a few members of OMF assemblages 2014, 2015a; Waud et al., 2016b). Therefore, the co-occurrence can promote the growth and flowering of orchids under various of terrestrial orchids observed in nature may be mediated by environmental stresses (McCormick et al., 2009, 2018). Therefore, spatial distribution and interactions of the associated OMF. However, the identities of OMF and their interactions with the environment minimal research has been conducted on the relationship between may make certain orchid–OMF assemblages more beneficial the spatial distribution of epiphytic orchids on different phorophytes to the growth of orchids, positively affecting their distribution and OMF. Since epiphytic orchids account for about 70% of and population dynamics. In addition, Nurfadilah et al. (2013) orchids (Dearnaley et al., 2012; Chase et al., 2015), the lack of found that fungi associated with some widely distributed such research limits our understanding of how OMF affect the Australian orchids were more likely to acquire nutritional distribution and population dynamics of orchids. resources than fungi associated with orchids found only in certain habitats. This has also been confirmed at the genotype level by subsequent multi-omics studies (Kohler et al., 2015; ROLES OF TULASNELLA IN ORCHID Fochi et al., 2017a,b). Interestingly, Tulasnella and some COMMUNITY CONSTRUCTION Serendipita fungi lack genes for using nitrate and nitrite, though these genes are commonly found in Ceratobasidium. Moreover, The fungi Tulasnella mostly reside in various orchid tissues (mainly these three types of rhizoctonias possess different genes that roots and stems) and tend to be extremely sensitive to environmental help in the absorption of carbon substrates. Accordingly, recent variables, indicating a strong dependence on host orchids or tests on the sensitivity of orchid seed to nitrate concentration surrounding plants. Therefore, recovery from disruption of the have revealed that nitrates can affect the distribution of orchids multi-nutrient balance among Tulasnella, orchids, and accompanying by directly inhibiting seed germination (Figura et al., 2020). plants (the plant species that often occur around a certain orchid Hence, nitrates have inhibitory effects on seed germination, species and do not belong to the Orchidaceae in natural habitats growth, and persistence of orchids. With the change of landscape, and are expected to have a specific association with the orchid the rapid increase in nitrate content in intensive pastures or species) that is established by long-term coevolution could meadows inhabited by a large number of orchid species due be difficult. This can result in orchid breeders or orchid enthusiasts to the high soil nitrification rate and the increasing atmospheric facing problems, while reestablishing conditions for growing orchids. nitrogen deposition around the world (Figura et al., 2020; Studies have shown that the use of peat-based, a mixture of Moore et al., 2020), and eutrophication of habitats (particularly coconut shells, bark shavings, soil from the original habitat, or in habitats with severe human disturbance, such as some ancient a mixture of pinecone scales, mosses, and humus, can induce tea estates in southwest China, the rich orchid resources are symbiosis between transplanted orchid individuals or asymbiotically faced with the impact of heavy use of chemical fertilizers and cultured orchid individuals grown ex situ and Tulasnellaceae fungi human destruction) poses a potential threat to the distribution (Han et al., 2016; Kaur et al., 2018; Qin et al., 2019). However, of orchids. It is worth mentioning that a recent study corroborated no Tulasnella symbiotic with orchid individuals were obtained that some Ceratobasidium symbionts can effectively alleviate when transplanted in original habitat soil or sawdust (May et al., the inhibitory effect of nitrate on orchid seed germination 2020; Li et al., unpublished data). Preliminary research suggests (Figura et al., 2021). In addition, recent evidence shows that that the dominant OMF and ONF in fungal communities some cyanobacteria species with nitrogen-fixing activities are reconstructed by cultured orchid individuals are different from present in the velamen of epiphytic orchids (Deepthi and Ray, those seen in wild populations. Overall, fungi belonging to the 2020). Therefore, in the epiphytic niches, Tulasnella and some groups Atractiellales, Auriculariales, Ceratobasidiaceae, and Fusarium Serendipita fungi that cannot use mineral nitrogen may benefit tended to increase, while the abundance of Tulasnellaceae and from the velamen roots of epiphytic orchids, at least during Pyronemataceae tended to decrease (Downing et al., 2017; Qin adulthood; indicating that the notion that OMF are free-living et al., 2019; May et al., 2020), as a consequence of transplantation, fungi may need to be reviewed, because epiphytic orchids may and the extent of such changes may depend on the time scales indirectly affect OMF performance by recruitingof culture or transplantation. This indicates low survival rates of cyanobacteria species. cultured orchids, which may be caused by the loss of some key

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OMF (e.g., Tulasnellaceae fungi) or the restricted construction found that OMF isolated from orchid species that coexist with of new mycorrhizal communities. Hence, selecting substrates with G. conopsea in the wild do not promote its seed germination high OMF diversity, using molecular identification of OMF and protocorm formation in vitro, since they require specific OMF. composition of substrates, is critical for improving culturing Environmental filtering largely accounts for the narrow practices. However, further research is required to determine the distribution of OMF associated with these generalist mycorrhizal extent of similarity in Tulasnella taxa between cultivated and wild orchids. Recent evidence indicates that phosphorus content is orchids across different time scales. higher in the roots of larger populations of Platanthera cooperi and the surrounding bulk soil, which are mainly colonized by the Tulasnellaceae. In contrast, higher zinc content and a A FRAMEWORK FOR HOW OMF higher relative abundance of Ceratobasidiaceae are observed AFFECT THE DISTRIBUTION AND in smaller P. cooperi populations (Kaur et al., 2020). Interestingly, POPULATION DYNAMICS OF ORCHIDS Ceratobasidiaceae are more abundant in phosphorus-rich restored grasslands, while Serendipitaceae are more common in semi- Orchid mycorrhizal fungi exhibit widespread biogeographical natural grasslands with higher organic matter content (Vogt- distributions with major clades found all over the world, suggesting Schilb et al., 2020). This may be due to differences in how that the widespread distribution of orchids is driven by OMF variables in a particular habitat are weighed. In addition, it (Jacquemyn et al., 2017). However, the mechanisms by which has been widely reported that several environmental variables OMF affect the distribution and population dynamics of orchids (such as soil water content, pH, and soil nitrogen content) are still poorly understood since most current knowledge is can affect the composition and abundance of OMF communities based on molecular data from adult plant symbionts, while (Jacquemyn et al., 2015a; Waud et al., 2017; Duffy et al., 2019; complex mycorrhizal associations with orchids occur at different Kaur et al., 2019; Mujica et al., 2020). Hence, the structure stages of their life cycle. In this paper, we postulate a simple of OMF communities is significantly related to framework for the effects of OMF on orchid distribution and microenvironmental changes. Thus, these factors exert a joint population dynamics, though this conception may be biased. effect on the formation and structure of orchid populations. We argue that orchid–OMF associations exhibit complementary It must be noted that this framework applies mainly to and specific effects of selection that are highly adapted to the terrestrial orchids. Since orchid–OMF interactions are of a higher environment, and promote the niche breadth of orchid species, order due to the presence of abundant phorophytes in epiphytic which may act as a stabilizing force. More specifically, orchid orchids, equilibrium dynamics underlying their mutual selection species with specific mycorrhizae are usually symbiotic with are complicated. More scenarios need to be considered to address generalist OMF, while OMF associated with host orchids with this problem though a recent study has shown that phorophytes generalist mycorrhizae are often limited in their distribution. and epiphytic orchids harbor different fungal communities (Eskov In other words, the distribution of orchids is shaped by coupled et al., 2020). Moreover, there should be greater focus on the influences of environmental variables and efficient complementary fungal taxa associated with epiphytic orchids, epiphytic niches, selection between OMF and orchids. The most well-known and accompanying plants as well as their mutual selection example of association between generalist OMF and orchid mechanisms. Lastly, the orchid–OMF complementary selection species with mycorrhizal specificity is that of Serendipitaceae, mechanisms may be related to evolutionary constraints, which which are symbiotic partners specifically associated with many will be discussed in detail in the following section. host orchids. Serendipitaceae are also widely distributed, shared In summary, the patchy distribution, heterogeneous by orchids and their accompanying plants in several habitats, abundance, identities, and spatiotemporal variability of OMF or serving as a beneficial growth-promoting fungus for a wide have crucial effects on the local distribution and population range of agricultural crops (e.g., Davis et al., 2015; Jacquemyn dynamics of orchids. The local distribution of orchids may in et al., 2015a; Fritsche et al., 2020; Reiter et al., 2020). While turn promote the formation and diversification of orchid species Platanthera leucophaea, which is protected by the United States by curtailing the population size and gene flow among federal government, is highly dependent on Ceratobasidium in populations, which may be responsible for the huge species the tallgrass prairie ecosystems of North America, Ceratobasidium diversity of Orchidaceae. Since the distribution of orchids is species has also been isolated from various orchid species found affected by various factors, the relationship between OMF and in other locations (Thixton et al., 2020). Similarly, two rare the distribution of orchids should be further explored. Future Orchis sister species have high specificity for the dominant fungal studies must particularly focus on the influence of availability symbiont Tulasnella helicospora, even though this fungus is found of OMF, flow of nutrient resources between orchids and OMF, across the world (Calevo et al., 2020). Contrarily, generalist and abiotic factors on the distribution of tropical orchids. mycorrhizal orchids recruit a large number of symbiont partners, but these compatible OMF are rarely found in other areas (Jacquemyn et al., 2011a). While biogeography is the main factor PHYLOGENETIC SIGNALS IN ORCHID– affecting the microbial communities (including fungi and bacteria) OMF INTERACTIONS associated with Gymnadenia conopsea (i.e., composition varies greatly with location), the species still exhibits certain specificities The composition and distribution of biological assemblages are (Lin et al., 2020; Xing et al., 2020a). Similarly, Gao et al. (2020) strongly influenced by a series of ecological and evolutionary

Frontiers in Plant Science | www.frontiersin.org 6 May 2021 | Volume 12 | Article 647114 Li et al. Roles of OMF in Orchid Distribution processes (Heilmann-Clausen et al., 2016; Boeraeve et al., 2018; phylogenetic signals in both orchids and fungi (Xing et al., Beng and Corlett, 2019; Wang et al., 2019a). The genetic relationship 2019). Moreover, no significant differences were observed in between hosts in antagonistic or mutualistic interactions and phylogenetic signals between the three types of orchids and its influence on the assembly of fungal communities has been the sub-networks formed by rhizoctonias or Tulasnella separately, unraveled by recent studies (e.g., Põlme et al., 2013; van der which were close to zero. Differences in the results of these Linde et al., 2018). For example, different degrees of evolutionary two studies could be related to the phylogenetic spectra of constraints have been observed in AM, EcM, plant pathogens, the orchids involved (Tedersoo et al., 2014; Xing et al., 2019). and fungi in general (Erlandson et al., 2018; Wang et al., 2019a,b; The number of terrestrial, epiphytic, and lithophytic orchid Yang et al., 2019). In addition to these biotrophic fungal guilds, species in the latter study was less than 20, and the phylogenetic the dissimilarities among free-living soil fungal communities diversity focused on fewer orchid genera. No significant significantly increase over large spatial scales and with increasing phylogenetic signals were consistently detected on either side plant phylogenetic distance, however, the explained variation is of the interactions in the binary network formed by seven relatively lower than that of pathogens and EcM fungi (Yang species of orchids and rhizoctonias belonging to different genera et al., 2019). Controlled experiments also suggest that soil distributed in Song Mountain, Beijing (Chen et al., 2019b). microorganisms that are obligately symbiotic with some trees Thus, further research could sample greater numbers of different usually promote growth on these trees or closely related species, types of orchids focusing on the broader orchid phylogenetic but do not affect growth as much on distantly related species spectra. Furthermore, the associations of phylogenetically related (Liang et al., 2019). These results suggest that closely related host orchids with similar fungal communities in rhizosphere hosts usually have certain fungal specificities. Considering the soil and orchid-occupied bulk soil may be worth investigating. dependence and specificity of orchids on OMF, the evolution The phylogenetic niche conservatism theory proposes that host of host orchids may be a key factor affecting the composition species with close genetic relationships tend to possess highly of the OMF community. similar morphologies and functions (Losos, 2008). There is In recent years, some studies have indicated the existence substantial evidence for the effects of phylogenetic eigenvectors of phylogenetic conservatism in the interplay between orchids and species-specific functional traits on fungal communities often and OMF. Jacquemyn et al. (2011b) revealed that the phylogenetic overlap significantly. The phylogenetic effects of hosts can structure of 16 species of the genus Orchis distributed across be explained by the conservatism of plant functional traits. In 11 different regions in Europe can explain the community addition, the phylogenetic relatedness of hosts could explain the differences in associated Tulasnellaceae. Many orchid species similarity of functional traits to a large extent, which would allow that are closely related within genera host similar rhizoctonias a rough prediction of either of these features based on the other or Tulasnellaceae operational taxonomic units (OTUs), such as (Wardle et al., 2004; Legay et al., 2014; López-García et al., 2017; Cypripedium (Shefferson et al., 2007), Goodyera (Shefferson et al., Wang et al., 2019a; Yang et al., 2019). This is probably one of 2010), Neottia (Těšitelová et al., 2015), Teagueia (Suárez and the major reasons for the greater likelihood of observing phylogenetic Kottke, 2016), Caladenia (Phillips et al., 2016), Dendrobium signals from the same orchid genus during interactions with (Xing et al., 2017), Pleione (Qin et al., 2019), and Cypripedioideae rhizoctonias. However, since data regarding root traits that are (lady’s slipper subfamily; Shefferson et al., 2019). Therefore, important in the construction of underground communities is orchid–OMF specific associations during their evolutionary history lacking, further investigations are required to examine the extent may result in strong influences of orchid phylogeny on OMF to which evolutionary constraints of orchid genera are caused by communities. However, rhizoctonias display little or no coevolution their own functional traits. In addition, little to no phylogenetic with host orchids. This indicates asymmetric interactions during signals were observed in the narrow phylogenetic spectra of coevolution process and phylogenetic conservatism of functional orchids. This could be because the associated rhizoctonias were traits of orchids (De Deyn and van der Putten, 2005; Heilmann- mostly saprotrophic and endophytic fungi (Smith and Read, 2008; Clausen et al., 2016; Wang et al., 2019a). Jacquemyn et al., 2017) with relatively high functional redundancy Nevertheless, studies on the interactions between orchids (particularly saprotrophic fungi) and sensitivity of local species of multiple genera and rhizoctonias have produced inconsistent pools to abiotic environmental filtering, which would substantially conclusions. Martos et al. (2012) performed a phylogenetic obscure the influence of orchid phylogeny (Setälä and McLean, 2004; analysis of tropical orchids and symbiotic rhizoctonias distributed Erlandson et al., 2018). on Reunion Island, utilizing a narrow resolution (34 angraecoid When a plant invades or is transplanted into a new environment, species) and a broader resolution (25 orchid genera), and existing microorganisms in the environment may adapt or showed that the overall phylogenetic signal was weak. At a be redistributed. Over time, the outcomes of these adaptations narrow resolution, the evolutionary constraints between orchids may not be very beneficial to hosts of other genotypes (Batstone and rhizoctonias tended to be asymmetric, with phylogenetic et al., 2020), which indicates that shared evolutionary history signals only observed in orchids. Interestingly, at the broader is an important factor in the mutual selection between hosts resolution, both orchids and rhizoctonias in the epiphytic and microorganisms. Consistent with this view, recent studies sub-networks displayed significant phylogenetic signals. Similarly, have shown that “invasive orchids were capable of associating a recent analysis of the mycorrhizal association of 44 tropical with a broader range of mycorrhizal fungi than co-occurring orchids covering three life forms (terrestrial, epiphytic, and native congeners (a generalist strategy)” but they were also less lithophytic) with rhizoctonias or Tulasnella, revealed low likely to harbor pathogenic fungal groups (Downing et al., 2020).

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However, continual monitoring on longer time scales is required insight into complex mycorrhizal symbiotic relationships. to verify whether beneficial associations developed by invasive Immediately afterward,Martos et al. (2012) built a binary orchids are driven by evolutionary history. network of nearly half of the tropical orchid species and 95 Hence, to summarize these two sections, the composition of rhizoctonia fungi associated with them on Reunion Island, OMF communities are determined jointly by ecological and and found that the overall orchid mycorrhizal network showed evolutionary constraints, the relative importance of which depends high modularity due to the ecological barrier between epiphytic on the specific time, space, and orchid species studied. Subsequent and terrestrial orchids. However, the epiphytic subnetwork case studies could determine the contributions of these constraints formed a highly nested pattern. This study constructed the through variation partitioning analysis (VPA) and help us largest orchid mycorrhizal network to date, which was another understand the relationship between orchid ecology and evolution. important milestone in the progress of the orchid mycorrhizal network and continues to influence fields other than orchid mycorrhizal networks (Figure 1C). Subsequently, three studies ORCHID MYCORRHIZAL NETWORK further supported the highly modular structure of the orchid mycorrhizal network. The structure of the mycorrhizal network, The architecture of plant–fungus interactions varies according formed by species of the genus Dactylorhiza with different to the mycorrhizal type. The association network of AM and levels of ploidy and inhabiting a wide range of habitats (including plants is usually characterized by a nested assembly such that acid peat bogs, wet alkaline grasslands, dry meadows, and host plants that are symbiotic with fewer AM prefer to form forests), is characterized by modularity that is significantly symbiotic associations with AM that are symbiotic with most dependent on local environmental conditions (Jacquemyn et al., host plants (Chagnon et al., 2012; Montesinos-Navarro et al., 2016b). Although orchid species of different life forms are all 2012). Orchid mycorrhizae and ericoid mycorrhizae (ErM) simultaneously symbiotic with multiple OMF, the overall interaction networks form a modular structure (Martos et al., interconnected network remains highly modular due to the 2012; Jacquemyn et al., 2015b; Toju et al., 2016; Xing et al., enhanced specificity of Tulasnellaceae from terrestrial to epiphytic 2019) with high specificity between host plants and partners, or lithophytic orchids (Xing et al., 2019). Interestingly, overall while EcM network architectures tend to assume an intermediate OMF diversity in a narrow transect of 10 × 1,000 m with structure (Bahram et al., 2014; van der Heijden et al., 2015). relatively similar habitats could be partitioned into a subset Recently, Põlme et al. (2018) performed a meta-analysis of of 20 terrestrial orchids with mycorrhizal diversity belonging 111 datasets of plant–fungus interactions, which showed that to five coexisting genera, low overlap among the subsets, and the OMF community responded most strongly to orchid host multiple isolated groups present in the interconnected network identity, with significantly higher levels of specificity than other (Jacquemyn et al., 2015b). types and higher modularity than EcM and AM. In general, In contrast, four studies supported significantly nested the orchid mycorrhizal network has significant characteristics network features. The nested network formed between the of modules as a whole. However, the contributions of modularity highly diverse epiphytic orchids and rhizoctonia distributed and nestedness in the local network often change, and the in tropical montane rainforests of southern Ecuador may orchid–OMF interaction in different ecosystems shows be influenced by climate, as climate is the main driving force inconsistency with the whole in network eigenvalues. Temperate for OMF community turnover among sites (Kottke et al., and Mediterranean ecosystems exhibit slightly different 2013). Herrera et al. (2018) further confirmed that terrestrial architectures: the former tends to be significantly nested and epiphytic orchids shared abundant Tulasnellaceae mycobionts (Jacquemyn et al., 2011a, 2015b, 2016b), whereas tropical orchids in different habitats within tropical forests of southern Ecuador, and OMF symbiosis are more diversified Martos( et al., 2012; and the network showed a nested structure with generalists Kottke et al., 2013; Herrera et al., 2018; Xing et al., 2019, 2020b). forming the core. Due to the large degree of overlap seen in The distribution of orchid species and OMF and their the mycorrhizal communities of epiphytic and lithophytic selective effects constitute a complex orchid mycorrhizal network, orchids, the network structure formed by these two types of and the tight junctions present in the network are particularly orchids and sympatrically distributed terrestrial orchids is important for the coexistence and population dynamics of highly modular but also shows significant nestedness Xing( orchid species. Jacquemyn et al. (2011a) applied network analysis et al., 2019; Qin et al., 2020). Notably, the OMF network of for studying symbiotic relationships between orchids and OMF Dendrobium species inhabiting the same phorophyte escaped for the first time, and analyzed the architecture of the interaction strong selection by the host and showed significant asymmetric between 16 Orchis species distributed in 11 regions of Europe specialization (Xing et al., 2020b). In addition, consistent with and OMF. From this study, they confirmed that the interaction pollination networks, robustness analysis revealed that generalist between orchids and OMF at the community level showed a OMF and orchid species play an important role in the stability nested structure similar to a mutualistic relationship network of interrelated networks, and their loss may drive the cascading seen in pollination and seed dispersal, as well as networks of loss of biodiversity (Memmott et al., 2004; Burgos et al., 2007; predation. This study was identified as a pioneering work in Herrera et al., 2018). Moreover, the robustness of the symbiotic the field of orchid mycorrhizal networks based on our LCS network formed by terrestrial and epiphytic orchids was only analysis (Figure 1B). To our knowledge, this is also one of slightly different, implying that OMF is equally important for the first studies to apply network analysis methods to provide the fate of both life forms of orchids (Herrera et al., 2018).

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FORMATION OF SIGNIFICANTLY be due to the specific selection of OMF taxa by host orchids NESTED STRUCTURES (Jacquemyn et al., 2015b; Xing et al., 2019). In order to maximize mutual symbiosis in a complex environment, hosts usually allocate Although there was no significant difference in community more carbohydrates to better quality partners, resulting in increased nestedness among different mycorrhizal types, it was levels of specificity for the association between orchids and OMF, significantly negatively correlated with annual average rainfall. which in turn form a symmetrical and modular network structure Moreover, the nestedness values of orchid mycorrhizal networks of interactions (Kiers et al., 2011). Notably, the host selection showed large variation, implying that the significant nested effect of ErM associations is low but still presents a high degree structures formed by orchids and OMF may be more sensitive of modularity, which may be explained by the high sensitivity to fluctuations in environmental conditions Põlme( et al., of the modularity metric to total links in the dataset (Bahram 2018). This is consistent with the hypothesis proposed by et al., 2014). Moreover, the modularity of networks may be due Kottke et al. (2013) that climate may be the cause of nested to environmental variables that enhance specific selection of OMF networks. More specifically, the similarity of OMF communities by hosts (Jacquemyn et al., 2010b; Shefferson et al., 2019). Specific resulting from habitat variation may explain the observed environmental gradients or distinct niche differentiation may allow nested structure, such as the significant nested structure seen host orchids to be specifically associated with OMF characterized in Orchis species due to low variation in habitats. Contrarily, by greater taxonomic richness or functional diversity. In addition, Dactylorhiza species exhibit greater habitat differentiation, the presence of forbidden links may explain the strong modular resulting in rare overlap among OMF communities between structure (Olesen et al., 2011). For example, the inconsistency of different populations and a highly modular structure (Jacquemyn spatiotemporal dynamic changes in OMF limits certain pairwise et al., 2011a, 2016b). From an evolutionary point of view, interactions that may occur throughout the network. mycorrhizal associations of some species of Orchis and Cypripedium may be undergoing expansion of phylogenetic breadth, presenting broad specificity, and gradually driving A FRAMEWORK FOR WEIGHING THE network attributes to have generalists at the core order to RELATIVE IMPORTANCE OF maximize adaptation to the environment and absorb nutrients NESTEDNESS AND MODULARITY (Shefferson et al., 2007; Jacquemyn et al., 2011b). In addition, the research scale and the threshold for species Based on these factors that affect the characteristics of the delimitation may be two important factors affecting network orchid mycorrhizal network, we initially proposed a framework nestedness. The smaller the scale of the network constructed, the to weigh the relative importance of nestedness and modularity tighter interaction within the network, resulting in increased of the orchid mycorrhizal network (Figure 2). The characteristics nestedness of the network (Caruso et al., 2012; Öpik and Moora, of complex mycorrhizal networks formed by orchids and widely 2012; Chagnon et al., 2016). Thus, sampling should be performed distributed OMF mainly depend on the relative strength between at the similar scales to compare the mycorrhizal network of specific selection of host orchids and generalist selection of coexisting orchid species in different habitats. As the OTU sequence OMF. When the coupled influences of phylogenetic spectra, similarity threshold increases, the number of OTUs and rare root traits, and environmental differences of orchids increases associations increase, while the strength of nestedness decreases the intensity of specific selection of host orchids beyond that (Toju et al., 2014; Põlme et al., 2018). However, the pattern of by OMF, the network structure is highly modular. Contrarily, nestedness observed in the orchid mycorrhizal network did not when the similarity of environmental conditions drives coexisting vary according to the OTU delimitation threshold, probably because orchid species to share similar OMF communities, resulting most of the OMF considered in these studies were highly abundant in greater intensity of generalist selection of OMF, the network species (Jacquemyn et al., 2011a; Herrera et al., 2018). Considering structure shows significant nested assembly. the importance of rare species in subsurface ecosystem services, the impact of OTU classification on network nestedness should be fully considered, while performing in-depth analysis of orchid– FUTURE DIRECTIONS fungal (including ONF) networks. Co-occurrence network analysis is a promising method to gain insight into ecological communities and may serve as a potential FORMATION OF HIGHLY MODULAR approach to more efficiently and conveniently study the FEATURES distributions of microorganisms, the pattern of symbiotic relationships, and their impact on plant distribution and population Since coexisting orchid species commonly exhibit highly spatially dynamics at the community level. However, this method has clustered and strongly spatially segregated distribution patterns not been fully applied to multiple mutualisms of orchids, fungi, and are often associated with different OMF communities, and and their accompanying plants or phorophytes. Therefore, more these OMF communities with patchy distributions rarely overlap attention should be paid to the in-depth analysis of the total (Jacquemyn et al., 2007, 2014; Waterman et al., 2011; Waud et al., fungal co-occurrence network among different habitats 2016b), the interaction network between orchids and OMF often (populations) of the same species, different orchid species coexisting shows highly modular characteristics. On the one hand, this may in the same habitat, and orchid species of different life forms

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FIGURE 2 | A framework of the architecture of the orchid mycorrhizal network. The intensity between the specific selection of host orchids and the generalist selection of orchid mycorrhizal fungi (OMF) indirectly determines the relative importance of modularity and nestedness by affecting the degree of similarity of OMF communities. The thick line implies that the phylogenetic conservatism and root traits of host orchids as well as environmental variables jointly drive OMF to be significantly more specific than ectomycorrhizae (EcM) and arbuscular mycorrhizae (AM) fungi. or at different developmental stages in further studies. In order Shah et al., 2019; Fritsche et al., 2020). Interestingly, these to increase the accuracy of orchid fungal networks, spatial rare OMF coexist with a wide range of plants and increase autocorrelations should be avoided as far as possible when the reproduction and fitness of symbiotic hosts. Moreover, collecting samples and, combinations of analytical methods should S. indica has value in agricultural applications due to its effect be used. Moreover, analytical methods such as IDEN should on increasing yield of tomatoes by 65%, while also inducing be developed for the investigation of orchid traits and examining their resistance to salt stress (Abdelaziz et al., 2019). bipartite networks of orchid–fungus interaction, which can help Increasing attention to the mycorrhizal network of orchids, understand cross-kingdom associations between vegetation data rare taxa in the network, and adaptive evolution between and microorganisms (Feng et al., 2019). Alternatively, interactions orchids and fungi helps identify functions of key orchid fungi among orchid-associated fungi can be jointly analyzed by MENA and provides clues about orchid distribution, population and SparCC, using CoNet, which comprehensively considers dynamics, and the mechanisms underlying orchid–fungal multiple correlations, or SPIEC-EASI, which uses a more inferential mutualisms. Thus, such studies may lend insight into the function (Deng et al., 2012; Faust et al., 2012; Friedman and following aspects with significant implications: Alm, 2012; Kurtz et al., 2015). The abundance of microorganisms in a local community 1. Since the protective effect of mycorrhizal symbiosis on plants is extremely uneven, as shown by a few dominant groups is a redundant feature, some key taxa revealed by network playing major roles in active growth along with a large number analysis can be used as targets. The isolation and culture of rare groups (Jia et al., 2018). To distinguish abundant and of these target strains can be achieved as far as possible rare microbes in a community in terms of their roles and using medium prediction techniques in combination with contributions, all OTUs detected within a community are usually some characteristics of target strains (such as the increase divided into six exclusive categories based on relative abundance in the proportion of rare microorganisms in acidic (Figure 1D; Dai et al., 2016; Chen et al., 2019c). Recently, environments) or simulating the growth conditions of orchids an increasing number of studies have emphasized the importance in the field. In addition, the effects of their combinations of rare biosphere microbes, which includes more metabolically on orchid germination and various growth stages can active microorganisms than abundant groups, plays a key role be examined to identify simplified microbial groups that in co-occurrence networks, ecosystem versatility, and plant dominate the community and can meet the demand for performance. These microbes are not only highly resistant to host nutrients. Tentative exploration of orchid SynCom is environmental stresses, but also enhance the function of abundant would be a major advancement in orchid microbiome research microbes to some extent (Jousset et al., 2017; Ziegler et al., and a key step for the application of scientific research 2018; Liang et al., 2020; Xiong et al., 2020). Similarly, some achievements into greenhouse and natural environments. rare OMF affiliated with Serendipitaceae (such as Serendipita 2. Metagenomic analysis can assist in the functional study of key indica and Serendipita restingae) have been demonstrated to species, and binning assembly with the help of contigs obtained promote the germination of orchid seeds and the growth and by metagenomic splicing can help in the annotation of genes adaptation of plantlets (Schäfer and Kogel, 2009; Oliveira et al., 2014; and their functions. Moreover, comparative genome analysis

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and evolutionary analysis of inseparable key species at the 5. Increasing evidence suggests that nitrates significantly affect strain level may benefit from such approaches and advance the composition and abundance of OMF and inhibit the our understanding of the mechanisms of ecological adaptation, germination of orchid seeds in natural habitats (Duffy et al., nutrient mutualism, and metabolic functions of the strains. 2019; Figura et al., 2020). Further work should focus on the 3. Since plant roots continuously secrete carbon and other effects of specific environmental variables, such as soil moisture nutrients to the rhizosphere environment, the rhizosphere content, nitrate content, and pH, which are frequently reported is known as one of the most dynamic interfaces on Earth. to affect OMF communities in network analyses, to gain insight This significantly affects the arms race within complex into how these metrics affect sub-modules and the entire microbial communities as well as the growth and health network. At the same time due to the lack of reports on of hosts (Jogaiah et al., 2013; Raaijmakers, 2015; Lee et al., orchid seed-associated microbial communities, we know little 2020). However, reports on fungal communities in the to nothing about the heritability of microorganisms associated rhizosphere of orchids are currently limited. Therefore, future with orchid species and the vertical transmission ability of the studies should focus on the composition, dynamics, and microbiome at the plant level. These are important aspects of function of orchid fungal communities in this microdomain orchid–fungus mutualism that require urgent attention. and the correlation of their biogeographic patterns with the distribution and population dynamics of orchids. Finally, in order to better point out the research direction 4. Attempts should be made to correlate the underground of orchid fungal networks, while emphasizing the importance fungal diversity with the genetic characteristics of aboveground of considering ONF and making full use of network analysis orchid populations to gain insight into the genetic diversity methods in orchid–fungal interaction, we also provide a conceptual and dynamic history of orchid populations. This can be done framework illustrating that orchid fungal networks are critical through SSR molecular markers and ABC models or SNP for insight into the complex and dynamic linkages between the markers and DADI models, to indirectly predict the dynamics orchid, fungi, and the environment, as well as the exploration of fungal diversity with the aim of protecting orchid gene of orchid conservation practices (Figure 3). Furthermore, several pools (including orchid provenances and fungal sources). forward-looking studies have recently confirmed that certain

FIGURE 3 | A framework illustrating that orchid fungal networks are critical for insight into the complex and dynamic linkages between the orchid, fungi, and the environment, as well as the exploration of orchid conservation practices. The thick lines imply increasing evidence that environmental factors may indirectly affect orchid distribution and population dynamics by driving niche partitioning in OMF communities (see the second paragraph in the Introduction); dashed line with question marks indicate hypothetical relationships that have rarely been studied.

Frontiers in Plant Science | www.frontiersin.org 11 May 2021 | Volume 12 | Article 647114 Li et al. Roles of OMF in Orchid Distribution bacterial taxa as well as microbial interkingdom interactions are FUNDING essential for plant growth (Durán et al., 2018; Finkel et al., 2020). Observations under the microscope suggest that bacterial This work was supported by the National Natural Science taxa mainly reside within the root caps of orchids, while fungal Foundation of China (Grant No. U1702235) and the Yunnan taxa are found in various subdivisions of roots. The spatial University’s Research Innovation Fund for Graduate Students distribution pattern of such cross-kingdom microorganisms in (Grant No. 2019z052). roots seems to be consistent with their characteristics because fungal hyphae can act as highways for bacterial movement and also as transport systems for microorganisms belonging to other ACKNOWLEDGMENTS kingdoms. However, it is unclear whether microorganisms in different kingdoms engage in mutualism within the roots, and We thank all members of the Gao Laboratory for their selfless whether such mutualism affects the distribution and population help and support in the process of literature collection, discussion dynamics of orchids. These issues should be focus areas of and writing, and apologize to all those colleagues whose work research on orchids and other plants in the future. was not cited.

AUTHOR CONTRIBUTIONS SUPPLEMENTARY MATERIAL JG and M-AS designed the outline of the manuscript. TL, JG, SW, and WY collected the data and wrote the manuscript. The Supplementary Material for this review can be found online M-AS and JG polished the article. All authors contributed to at: https://www.frontiersin.org/articles/10.3389/fpls.2021.647114/ the article and approved the submitted version. full#supplementary-material

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The impact of life form on the architecture of orchid mycorrhizal networks in tropical forest. Oikos 128, 1254–1264. doi: 10.1111/oik.06363 Copyright © 2021 Li, Wu, Yang, Selosse and Gao. This is an open-access article Xing, X., Liu, Q., Gao, Y., Shao, S., Guo, L., Jacquemyn, H., et al. (2020b). distributed under the terms of the Creative Commons Attribution License (CC BY). The architecture of the network of orchid–fungus interactions in nine co- The use, distribution or reproduction in other forums is permitted, provided the occurring Dendrobium species. Front. Ecol. Evol. 8:130. doi: 10.3389/ original author(s) and the copyright owner(s) are credited and that the original fevo.2020.00130 publication in this journal is cited, in accordance with accepted academic practice. Xing, X. K., Ma, X. T., Men, J. X., Chen, Y. H., and Guo, S. X. (2017). No use, distribution or reproduction is permitted which does not comply with Phylogenetic constrains on mycorrhizal specificity in eightDendrobium these terms.

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